Our research is aimed at revealing the mechanisms by which aquatic animals, in particular fish, evolve in response to environmental challenges such as those imposed by climate change. Fish and aquatic invertebrates vary greatly with regard to their tolerance towards environmental perturbation. Our overall research question is: What is the mechanistic/ molecular basis for variable environmental stress tolerance? As comparative biologists we collaborate with many other laboratories to study aquatic species that inhabit extreme and fluctuating environments. We focus on biochemical mechanisms that confer high tolerance to environmental stress in fish. Both short-term (physiological plasticity) and long-term (genetic/ epigenetic adaptation) mechanisms are being studied. Most of our efforts are directed towards tilapiine cichlids and sticklebacks. These species complexes have rapidly conquered diverse habitats that differ greatly in the selection pressures that are being encountered during evolution. We are particularly interested in understanding how species with high tolerance to ecologically relevant climate parameters evolve from species with low tolerance. Key abiotic parameters of interest in our lab are salinity, temperature, and redox chemistry.

Cichlids

Cichlids are a family of perciform teleosts that have radiated into thousands of species, which are uniquely adapted to particular environmental niches. They are most abundant in Central and South America and in Africa. Cichlids of the Great Lakes in East Africa's Rift Valley have undergone the most rapid and expansive species radiation during vertebrate evolution. They represent a classical model for evolutionary biology . The complete genomes of many African cichlids have been annotated making them accessible for proteomics approaches . Many cichlids, in particular tilapiine species, have acquired extreme tolerance to salinity stress. For instance, the Black-chinned tilapia (Sarotherodon melanotheron) tolerates a salinity range from freshwater to 130 g/kg. It encounters these huge salinity fluctuations in extreme habitats such as the Saloum estuary in the Senegal . We are studying the biochemical mechanisms that set these extremely euryhaline fish apart from other, less tolerant, cichlids. We are also interested in the evolutionary trade-offs that prevent the majority of cichlids from "sliding down" an evolutionary path that favors euryhalinity and extreme salinity tolerance.

Sticklebacks

The order of stickleback fishes (Gasterosteiformes) is represented primarily by marine species. It includes pipefishes, sea needles, and sea horses. Some taxa of sticklebacks, in particular threespine and ninespine sticklebacks have conquered freashwater habitats by convergent evolution on all continents throughout the Northern hemisphere . They have been studied for more than a century because of their adaptatbility to diverse environments and thier interesting breeding bahvior . Major new concepts of behavioral biology have emerged from research on threespine sticklebacks . Threespine stickleback populations are classified into 3 different ecotypes (resdient marine, anadromous, and landlocked freshwater). They are also classified into 3 distinct morphotypes based, primarily, on their lateral body armor (fully plated - trachurus, partially plated - semiarmatus, low-plated or plateless - leiurus). Their genome has been sequenced and annotated . We are studying the mechanisms enabling rapid adaptation of threespine sticklebacks to habitats that impose environmental stress and strong selection pressure on these fish.

Coastal habitats & Salt Lakes

Euryhaline aquatic animals have mainly evolved in two extreme environments: coastal habitats (the intertidal zone and estuaries) and arid habitats (desert lakes, ponds, and creeks) . These environments are characterized by fluctuating salinity. Besides salinity stress, they also impose temperature, oxidative, and other types of stress on organisms. Examples of such habitats include coastal lagoons in California and elsewhere , the California Salton Sea , and Salt Creek in Death Valley . Primitive animals (rotifers, tardigrades, and nematodes) are even found in the diverse ponds of Bratina Island in the Dry Valleys region of Antarctica . Organisms inhabiting these environments are often eurytolerant, i.e. tolerant towards multiple environmental stressors. We are studying the underlying molecular basis for such environmental stress cross-tolerance. The goal is to know how many and which genes and proteins need to undergo evolutionary change to confer high environmental stress tolerance in aquatic animals. Such knowledge informs us about the time scale and mechanistic prerequisites that are necessary and sufficient for adaptation of aquatic organisms to salinity and temperature stress. Hence, this research will reveal animal coping strategies that have a selective advantage during anthropogenically accelerated climate change.

Stress proteome evolution

Evolution has given rise to fish species that are uniquely adapted to a wide variety of most extreme habitats. We study the biochemical and evolutionary mechanisms that facilitate such adaptation . We aim to better understand how the minimal stress proteome has evolved to interact with other proteins to facilitate high environmental stress tolerance in euryhaline fish . The ultimate goal of our research is to decipher the logic by which stress-responsive signaling networks control transcriptional and proteome regulatory networks . Comparative studies of these networks in euryhaline and stenohaline species reveals targets of evolution when environmental salinity stress represents a major selection pressure. To transform correlational networks into causality networks our approaches are based primarily on molecular phenotyping (quantitative proteomics, SWATH mass spectrometry ) and functional genomics (gene targeting, genome editing ). The proteome represents the sum of expressed proteins in a given tissue at a particular time. It signifies the ultimate link connecting the genomic blueprint with environmental context-dependent structure and function of an organism. The dynamic proteome directly determines higher order phenotypes (complex morphology, physiology, behavior) . Thus, proteomics approaches allow studies of organisms and their tissues as integrated systems rather than a single or few molecules/ traits at a time, which facilitates network analyses and network decomposition . The combination of quantitative proteomics with functional genomics approaches permits causal linkages of genotypes to phenotypes that are adaptive in extreme and fluctuating environments.